1 2 DR. DARA ASHLEY SATTERFIELD (Orcid ID : 0000-0003-3036-5580) 3 PROF. MARK D HUNTER (Orcid ID : 0000-0003-3761-8237) 4 DR. TYLER FLOCKHART (Orcid ID : 0000-0002-5832-8610) 5 6 7 Article type : Letters 8 9 10 Abstract: 150; Main Text: 5,000; Figures: 4; Tables: 0; References: 85 11 12 13 Migratory monarchs that encounter resident monarchs show life-history changes and 14 higher rates of parasite infection 15 16 Dara A. Satterfield,*1 John C. Maerz,2 Mark D. Hunter,3 D.T. Tyler Flockhart,4 Keith A. 17 Hobson,5 D. Ryan Norris,4 Hillary Streit,3 Jacobus C. de Roode,6 and Sonia Altizer1 18 19 20 21 1Odum School of Ecology, University of Georgia, Athens, GA 30602, USA; 22 [email protected]; [email protected] 23 2Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, 24 USA; [email protected] 25 3Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 26 48109, USA; [email protected]; [email protected] 27 4Departmment of Integrative Biology, University of Guelph, Guelph, ON N1G2W1, Canada; 28 [email protected]; [email protected] Author Manuscript 29 5Department of Biology, Western University, London, ON N6A5B7, Can.; [email protected] This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/ele.13144 This article is protected by copyright. All rights reserved 30 6Department of Biology, Emory University, Atlanta, GA 30322, USA; [email protected] 31 *Corresponding author: Smithsonian National Zoo, PO Box 37012, MRC 5503, Washington, DC 32 20013; 770-584-4965 33 34 Statement of authorship: DAS, SA, and JCM designed the study; DAS conducted fieldwork. 35 MDH, HS, DAS and JR conducted cardenolide analyses, KAH, DTTF, DRN and DAS conducted 36 isotope work, DTTF and DRN developed natal origin maps. DAS, JCM, and SA conducted the 37 statistical analyses. DAS and SA wrote the manuscript with revisions from all authors. 38 Data accessibility statement: Data will be archived in Dryad, should the paper be accepted. 39 Running title: Migrant-resident monarch interactions 40 41 ABSTRACT 42 Environmental change induces some wildlife populations to shift from migratory to resident 43 behaviours. Newly formed resident populations could influence the health and behaviour of 44 remaining migrants. We investigated migrant-resident interactions among monarch butterflies 45 and consequences for life history and parasitism. Eastern North American monarchs migrate 46 annually to Mexico, but some now breed year-round on exotic milkweed in the southern U.S. 47 and experience high infection prevalence of protozoan parasites. Using stable isotopes (δ2H, 48 δ13C) and cardenolide profiles to estimate natal origins, we show that migrant and resident 49 monarchs overlap during fall and spring migration. Migrants at sites with residents were 13 times 50 more likely to have infections and three times more likely to be reproductive (outside normal 51 breeding season) compared to other migrants. Exotic milkweed might either induce these states 52 or attract migrants that are already infected or reproductive. Increased migrant-resident 53 interactions could affect monarch parasitism, migratory success, and long-term conservation. 54 55 56 57 Author Manuscript 58 59 60 This article is protected by copyright. All rights reserved 61 Key words: Asclepias curassavica, cardenolide profile, Danaus plexippus, Ophryocystis 62 elektroscirrha, partial migration, reproductive diapause, stable isotopes, tropical milkweed, 63 migrant-resident interactions 64 INTRODUCTION 65 Wildlife populations that engage in partial migration include both migrant and resident 66 individuals, with migrants moving between habitats seasonally and residents remaining in the 67 same area throughout the year (Newton 2008; Chapman et al. 2011a, b). Migrants and residents 68 often differ in reproductive behaviour, body size, predation risk, and in some cases, pathogen 69 infection (Adriaensen & Dhondt 1990; Hendry 2004; Hebblewhite & Merrill 2009; Altizer et al. 70 2011). Seasonal migrants and residents can interact and share habitat for part of the year, as 71 reported for Canada Geese (Branta canadensis), wildebeest (Connochaetes taurinus), and other 72 species (Caccamise et al. 2000; Estes 2014; Chapman et al. 2012), and such interactions are 73 likely widespread across taxa, given the high incidence of partial migration in wildlife 74 populations (Chapman et al. 2011a). However, the ecological implications of migrant-resident 75 interactions represent a critical knowledge gap in migration biology (Chapman et al. 2011a, b; 76 Brodersen et al. 2008). Migratory animals that share habitat with residents could encounter 77 additional resources or mates, but they might also experience greater exposure to natural enemies 78 or factors that alter their behaviour and movement. 79 Examining the ecological consequences of migrant-resident relationships is important for 80 the conservation of migratory species (Chapman et al. 2011a), many of which are now 81 threatened (Wilcove & Wikelski 2008). Residency is becoming more common in some 82 populations (Berthold 1999; Griswold et al. 2011), as birds, ungulates, and other animals 83 establish or expand resident sub-populations due to habitat alteration, climate change, or 84 supplemental feeding (Sutherland 1998; Fiedler 2003; Partecke & Gwinner 2007; Jones et al. 85 2014). For instance, a partially migratory population of Great Bustards (Otis tarda) in Europe 86 has increasingly shown resident behaviours, a change linked to high mortality of migrants on 87 power lines (Palacín et al. 2016). Bats, storks, waterfowl, and numerous other species are 88 showing similar increases in residency (Baskin 1993; Tortosa et al. 1995, 2002; Van Der Ree et Author Manuscript 89 al. 2006). Quantifying the extent to which migrants overlap with and respond to growing resident 90 sub-populations could help improve population projections and inform whether interactions with 91 residents require mitigation. This article is protected by copyright. All rights reserved 92 One critical question is whether residents increase pathogen infection risk for migrants 93 that encounter them. Theoretical models and empirical studies have demonstrated greater 94 infection prevalence for residents compared to migrants in some cases (Cross et al. 2010; Akbar 95 et al. 2012; Poulin et al. 2012; Qviller et al. 2013; Hall et al. 2014). Seasonal migration can 96 reduce pathogen transmission through several mechanisms, including by periodically enabling 97 migrants to escape parasite-contaminated habitat (migratory escape; Folstad et al. 1991; Loehle 98 1995) and by causing disproportionate mortality or loss of infected individuals during strenuous 99 journeys (migratory culling; Bartel et al. 2011). In contrast, resident populations would not 100 experience these processes and, as a result, can suffer higher parasite burdens – with the potential 101 for transmission to migrants (Hines et al. 2007; Cross et al. 2010; Hill et al. 2012). 102 Another important question is whether resident animals and their habitats also alter 103 migrant behaviour, particularly movement. This might occur if resident areas induce migrants to 104 curtail their journeys or modulate the physiological states that facilitate migration. For instance, 105 changes in climate and food have enabled some bird populations to shorten their migrations by 106 using new wintering sites closer to breeding grounds (Elmberg et al. 2014; Teitelbaum et al. 107 2016). Sites with year-round residents (providing mates and breeding habitat) might similarly 108 allow shortened migrations. Further, resources at resident sites could modify the physiological 109 states that help animals undertake and survive strenuous journeys (e.g., atrophy of non-essential 110 organs; Dingle 2014). Past work suggested that many migrants initially ignore environmental 111 stimuli that could interrupt migration (Kennedy 1985; Dingle 2014), but this remains 112 understudied and may be distinctly different for males (Gatehouse 1997). Moreover, persistent 113 exposure to attractive resources and heightened risks of migratory journeys might modify this. 114 Here, we focus on the widely recognized monarch butterfly (Danaus plexippus), whose 115 annual migration has been well studied (Figure S1), to investigate whether migrants in Texas 116 encounter residents en route, and to ask whether differences in infection status or reproductive 117 behaviour are associated with these interactions. To conserve energy for migration, most 118 (although not all) monarchs postpone reproduction during fall and enter a hormonally-induced 119 state called reproductive diapause (Herman 1973; Brower et al. 1977) as they travel to Author Manuscript 120 overwintering sites in central Mexico (Urquhart & Urquhart 1978). In spring, these same 121 monarchs break reproductive diapause, mate, and return to the southern U.S. to lay eggs on 122 milkweed; their progeny and grand-progeny continue northward to recolonize the breeding range This article is protected by copyright. All rights reserved 123 (Malcolm et al. 1993; Miller et al. 2012; Flockhart et al. 2013). Past work indicated that this 124 annual journey reduces monarchs’ infection prevalence from the specialist protozoan